Speeding up anterior-posterior patterning of insects by differential initialization of the gap gene cascade

Abstract

Recently, it was shown that anterior-posterior patterning genes in the red flour beetle Tribolium castaneum are expressed sequentially in waves. However, in the fruit fly Drosophila melanogaster, an insect with a derived mode of embryogenesis compared to Tribolium, anterior-posterior patterning genes quickly and simultaneously arise as mature gene expression domains that, afterwards, undergo slight posterior-to-anterior shifts. This raises the question of how a fast and simultaneous mode of patterning, like that of Drosophila, could have evolved from a rather slow sequential mode of patterning, like that of Tribolium. In this paper, we elucidate a mechanism for this evolutionary transition based on a switch from a uniform to a gradient-mediated initialization of the gap gene cascade by maternal Hb. The model is supported by computational analyses and experiments.

Geometric models for robust encoding of dynamical information into embryonic patterns

“…This proposal is motivated by the recent suggestion in insects that different sets of enhancers control waves of gap genes at different phases of embryonic growth ( El-Sherif and Levine, 2016 ). Such assumptions explain the so-called ‘speed-gradient’ model suggested to explain the gene expression wave dynamics observed during AP patterning in the beetle Tribolium ( Zhu et al, 2017 ) (see Figure 1—figure supplement 2 ) and (with some additional assumptions) the more subtle gene expression dynamics observed during AP patterning in Rudolf et al, 2020 ; El-Sherif and Levine, 2016 . Using both gene-network and geometric formalisms, we characterize the types of bifurcations found in systems transitioning from a dynamic to a static regime.…”

Geometric models for robust encoding of dynamical information into embryonic patterns

“…This proposal is motivated by the recent suggestion in insects that different sets of enhancers control waves of gap genes at different phases of embryonic growth (El-Sherif & Levine, 2016). Such assumptions explain the so-called "speed-gradient" model suggested to explain the gene expression wave dynamics observed during AP patterning in the beetle Tribolium (Zhu et al, 2017) (see Figure 1-figure supplement 2) and (with some additional assumptions) the more subtle gene expression dynamics observed during AP patterning in (Rudolf, Zellner, & El-Sherif, 2020). Using both gene-network and geometric formalisms, we characterize the types of bifurcations found in systems transitioning from a dynamic to a static regime.…”

How enhancers regulate wavelike gene expression patterns: Novel enhancer prediction and live reporter systems identify an enhancer associated with the arrest of pair-rule waves in the short-germ beetleTribolium

“…Hence, new models of embryonic pattern formation need to be adopted, and concomitantly, new models of how enhancers work within these pattern formation models. Some of the authors have recently suggested a model that explains the generation of either periodic or non-periodic waves of gene expressions speed model (6,23,24,30,34). In this model, a morphogen gradient modulates the speed of either a molecular clock (to produce a periodic pattern) or a genetic cascade (to produce a non-periodic pattern).…”

“…In the flour beetle Tribolium castaneum ( Tribolium ), it has been shown that both pair-rule and gap genes are expressed as dynamic waves that propagate from posterior to anterior (20–24), much like how segmentation and Hox genes are expressed in vertebrates (6). Even pair-rule and gap genes in Drosophila , classically thought to be expressed stably, have recently been shown to undergo dynamic posterior-to-anterior shifts (25–29), a phenomenon that has been suggested to be an evolutionary vestige of outright gene expression waves (6,30–33).…”